Glu-44 in the amino-terminal α-Helix of yeast vacuolar atpase e subunit (Vma4p) has a role for VoV1 assembly

Journal of Biological Chemistry

Volumn 288, Issue 51, 2013, Pages 36236-36243

  Okamoto Terry, Haruko ^a   Umeki, Kaori ^a   Nakanishi Matsui, Mayumi ^a   Futai, Masamitsu ^a  

^a IWATE MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE-SCANNING MUTAGENESIS; V-ATPASE; VACUOLAR ATPASE;

AMINO ACIDS; CATALYST ACTIVITY;

GLUCOSE;

ADENOSINE TRIPHOSPHATASE; ALANINE; ASPARAGINE; ASPARTIC ACID; GLUTAMIC ACID; GLUTAMINE; PROTON PUMP; UNCLASSIFIED DRUG; VMA4P PROTEIN;

ALPHA HELIX; AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME SUBUNIT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION;

BIOENERGETICS; CONFOCAL MICROSCOPY; ENZYME CATALYSIS; PROTEIN ASSEMBLY; V-ATPASE; YEAST;

AMINO ACID SEQUENCE; GLUCOSE; GLUTAMIC ACID; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VACUOLAR PROTON-TRANSLOCATING ATPASES;

EID: 84890961521     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.506741     Document Type: Article

References (39)

1. Futai, M., Nakanishi-Matsui, M., Okamoto, H., Sekiya, M., and Nakamoto, R. K. (2012) Rotational catalysis in proton pumping ATPases: From E. coli F-ATPase to mammalian V-ATPase. Biochim. Biophys. Acta 1817, 1711-1721
2. +-ATPase in vesicular trafficking: Targeting, regulation and function. Curr. Opin. Cell Biol. 20, 415-426
3. Okamoto, H., Futai, M. (2013) Vacuolar-Type ATPases in Animal and Plant Cells in Encyclopedia of Biophysics (Roberts, G. C. K., ed) pp. 2719-2724, Springer-Verlag Berlin, Heidelberg, Berlin
4. Forgac, M. (2007) Vacuolar ATPases: Rotary proton pumps in physiology and pathophysiology. Nat. Rev. Mol. Cell Biol. 8, 917-929
5. Kane, P. M. (2006) The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol. Mol. Biol. Rev. 70, 177-191
6. Compton, M. A., Graham, L. A., and Stevens, T. H. (2006) Vma9p (subunit e) is an integral membrane Vo subunit of the yeast V-ATPase. J. Biol. Chem. 281, 15312-15319
7. Diepholz, M., Venzke, D., Prinz, S., Batisse, C., Flörchinger, B., Rössle, M., Svergun, D. I., Böttcher, B., and Féthière, J. (2008) A different conformation forEGCstator subcomplex in solution and in the assembled yeast V-ATPase: Possible implications for regulatory disassembly. Structure 16, 1789-1798
8. Oot, R. A., Huang, L. S., Berry, E. A., and Wilkens, S. (2012) Crystal Structure of the Yeast Vacuolar ATPase Heterotrimeric EGC(head) Peripheral Stalk Complex. Structure 20, 1881-1892
9. Oot, R. A., and Wilkens, S. (2010) Domain characterization and interaction of the yeast vacuolar ATPase subunit C with the peripheral stator stalk subunits E and G. J. Biol. Chem. 285, 24654-24664
10. Oot, R. A., and Wilkens, S. (2012) Subunit interactions at the V1-Vo interface in yeast vacuolar ATPase. J. Biol. Chem. 287, 13396-13406
11. Zhang, Z., Zheng, Y., Mazon, H., Milgrom, E., Kitagawa, N., Kish-Trier, E., Heck, A. J., Kane, P. M., and Wilkens, S. (2008) Structure of the yeast vacuolar ATPase. J. Biol. Chem. 283, 35983-35995
12. Rishikesan, S., Thaker, Y. R., and Grüber, G. (2011) NMR solution structure of subunit E (fragment E(1-69)) of the Saccharomyces cerevisiae V1VO ATPase. J. Bioenerg. Biomembr. 43, 187-193
13. Owegi, M. A., Carenbauer, A. L., Wick, N. M., Brown, J. F., Terhune, K. L., Bilbo, S. A., Weaver, R. S., Shircliff, R., Newcomb, N., and Parra-Belky, K. J. (2005) Mutational analysis of the stator subunit E of the yeast V-ATPase. J. Biol. Chem. 280, 18393-18402
14. Kane, P. M. (1995) Disassembly and reassembly of the yeast vacuolar H(+)-ATPase in vivo. J. Biol. Chem. 270, 17025-17032
15. Kane, P. M., and Parra, K. J. (2000) Assembly and regulation of the yeast vacuolar H(+)-ATPase. J. Exp. Biol. 203, 81-87
16. 0 domains of yeast vacuolar H+-ATPase is an unconventional glucose-induced effect. Mol. Cell Biol. 18, 7064-7074
17. Beyenbach, K. W., and Wieczorek, H. (2006) The V-type H+ ATPase: Molecular structure and function, physiological roles and regulation. J. Exp. Biol. 209, 577-589
18. Sumner, J. P., Dow, J. A., Earley, F. G., Klein, U., Jäger, D., and Wieczorek, H. (1995) Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J. Biol. Chem. 270, 5649-5653
19. Wieczorek, H., Beyenbach, K. W., Huss, M., and Vitavska, O. (2009) Vacuolar- type proton pumps in insect epithelia. J. Exp. Biol. 212, 1611-1619
20. Merzendorfer, H., Reineke, S., Zhao, X. F., Jacobmeier, B., Harvey, W. R., and Wieczorek, H. (2000) The multigene family of the tobacco hornworm V-ATPase: Fovel subunits a, C, D, H, and putative isoforms. Biochim. Biophys. Acta 1467, 369-379
21. Nakanishi-Matsui, M., Breton, S., Okamoto, H., Futai, M. (2012) Roles and Regulatory Mechanism of Proton Pumping V-ATPase in Spermatozoa and Epididymis Physiology in Testis: Anatomy, Physiology and Pathology (Nemoto, Y., and Inaba, N., eds.) pp. 53-72, Nova Science Publishers, Inc., Hauppauge, NY
22. Sun-Wada, G. H., Imai-Senga, Y., Yamamoto, A., Murata, Y., Hirata, T., Wada, Y., and Futai, M. (2002)Aproton pump ATPase with testis-specific E1-subunit isoform required for acrosome acidification. J. Biol. Chem. 277, 18098-18105
23. o ATPase determined by solution NMR spectroscopy. J. Bioenerg. Biomembr. 43, 447-455
24. Yamashiro, C. T., Kane, P. M., Wolczyk, D. F., Preston, R. A., and Stevens, T. H. (1990) Role of vacuolar acidification in protein sorting and zymogen activation: A genetic analysis of the yeast vacuolar proton-translocating ATPase. Mol. Cell Biol. 10, 3737-3749
25. Hayashi, K., Sun-Wada, G. H., Wada, Y., Nakanishi-Matsui, M., and Futai, M. (2008) Defective assembly of a hybrid vacuolar H(+)-ATPase containing the mouse testis-specific E1 isoform and yeast subunits. Biochim. Biophys. Acta 1777, 1370-1377
26. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691
27. Takeshige, K., Baba, M., Tsuboi, S., Noda, T., and Ohsumi, Y. (1992) Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol. 119, 301-311
28. Pullman, M. E., Penefsky, H. S., Datta, A., and Racker, E. (1960) Partial resolution of the enzymes catalyzing oxidative phosphorylation. 1. Purification and properties of soluble dinitrophenol-stimulated adenosine triphosphatase. J. Biol. Chem. 235, 3322-3329
29. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254
30. Blaber, M., Zhang, X. J., and Matthews, B. W. (1993) Structural basis of amino acid α helix propensity. Science 260, 1637-1640
31. Kane, P. M. (2005) Close-up and genomic views of the yeast vacuolar H+-ATPase. J. Bioenerg. Biomembr. 37, 399-403
32. Dechant, R., Binda, M., Lee, S. S., Pelet, S., Winderickx, J., and Peter, M. (2010) Cytosolic pH is a second messenger for glucose and regulates the PKA pathway through V-ATPase. EMBO J. 29, 2515-2526
33. Schnitzer, D., Seidel, T., Sander, T., Golldack, D., and Dietz, K. J. (2011) The cellular energization state affects peripheral stalk stability of plant vacuolar H+-ATPase and impairs vacuolar acidification. Plant Cell Physiol. 52, 946-956
34. Stewart, A. G., and Stock, D. (2012) Priming a molecular motor for disassembly. Structure 20, 1799-1800
35. Charsky, C. M., Schumann, N. J., and Kane, P. M. (2000) Mutational analysis of subunit G (Vma10p) of the yeast vacuolar H+-ATPase. J. Biol. Chem. 275, 37232-37239
36. Féthière, J., Venzke, D., Diepholz, M., Seybert, A., Geerlof, A., Gentzel, M., Wilm, M., and Böttcher, B. (2004) Building the stator of the yeast vacuolar-ATPase: Specific interaction between subunits E and G. J. Biol. Chem. 279, 40670-40676
37. Flannery, A. R., and Stevens, T. H. (2008) Functional characterization of the N-terminal domain of subunit H (Vma13p) of the yeast vacuolar ATPase. J. Biol. Chem. 283, 29099-29108
38. Jones, R. P., Durose, L. J., Findlay, J. B., and Harrison, M. A. (2005) Defined sites of interaction between subunits E (Vma4p), C (Vma5p), and G (Vma10p) within the stator structure of the vacuolar H+-ATPase. Biochemistry 44, 3933-3941
39. Lu, M., Vergara, S., Zhang, L., Holliday, L. S., Aris, J., and Gluck, S. L. (2002) The amino-terminal domain of the E subunit of vacuolar H(+)- ATPase (V-ATPase) interacts with the H subunit and is required for VATPase function. J. Biol. Chem. 277, 38409-38415